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Risk factors for aspiration pneumonia after definitive chemoradiotherapy or bioradiotherapy for locally advanced head and neck cancer: A monocentric case control study

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Chemoradiotherapy (CRT) and bio-radiotherapy (BRT) are recognized as standard therapies for head and neck cancer (HNC). Aspiration pneumonia after CRT or BRT is a common late adverse event. Our aim in this study was to evaluate the cause-specific incidence of aspiration pneumonia after CRT or BRT and to identify its clinical risk factors.

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R E S E A R C H A R T I C L E Open Access

Risk factors for aspiration pneumonia after

definitive chemoradiotherapy or

bio-radiotherapy for locally advanced head and

neck cancer: a monocentric case control

study

Sadayuki Kawai1, Tomoya Yokota1*, Yusuke Onozawa2, Satoshi Hamauchi1, Akira Fukutomi1, Hirofumi Ogawa3, Tsuyoshi Onoe3, Tetsuro Onitsuka4, Takashi Yurikusa5, Akiko Todaka1, Takahiro Tsushima1, Yukio Yoshida1,

Yosuke Kito1, Keita Mori6and Hirofumi Yasui1

Abstract

Background: Chemoradiotherapy (CRT) and bio-radiotherapy (BRT) are recognized as standard therapies for head and neck cancer (HNC) Aspiration pneumonia after CRT or BRT is a common late adverse event Our aim in this study was to evaluate the cause-specific incidence of aspiration pneumonia after CRT or BRT and to identify its clinical risk factors

Methods: We performed a retrospective analysis of 305 patients with locally advanced HNC treated by CRT or BRT between August 2006 and April 2015

Results: Of these 305 patients, 65 (21.3%) developed aspiration pneumonia after treatment The median onset was

161 days after treatment The two-year cause-specific cumulative incidence by CRT or BRT was 21.0% Multivariate analysis revealed five independent risk factors for aspiration pneumonia, namely, habitual alcoholic consumption, use

of sleeping pills at the end of treatment, poor oral hygiene, hypoalbuminemia before treatment, and the coexistence

of other malignancies A predictive model using these risk factors and treatment efficacy was constructed, dividing patients into low- (0–2 predictive factors), moderate- (3–4 factors), and high-risk groups (5–6 factors), the two-year cumulative incidences of aspiration pneumonia of which were 3.0, 41.6, and 77.3%, respectively Aspiration pneumonia tended to be associated with increased risk of death, although this was not statistically significant (multivariate-adjusted hazard ratio 1.39, P = 0.18)

Conclusion: The cause-specific incidence and clinical risk factors for aspiration pneumonia after definitive CRT or BRT were investigated in patients with locally advanced HNC Our predictive model may be useful for identifying patients at high risk for aspiration pneumonia

Keywords: Head and neck cancer, Aspiration pneumonia, Risk factor, Chemoradiotherapy, Case–control study

* Correspondence: t.yokota@scchr.jp

1 Division of Gastrointestinal Oncology, Shizuoka Cancer Center, 1007

Shimonagakubo, Nagaizumi, Sunto-gun, Shizuoka 411-8777, Japan

Full list of author information is available at the end of the article

© The Author(s) 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made The Creative Commons Public Domain Dedication waiver

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Chemoradiotherapy (CRT) is a standard treatment for

lo-cally advanced head and neck cancer (HNC) [1]

Radiother-apy (RT) with cetuximab, defined as bio-radiotherRadiother-apy

(BRT), is also considered as a treatment option for patients

with locally advanced HNC [2] Compared with radical

sur-gery, CRT and BRT have an advantage of preserving organ

function and patients’ quality of life; however, their

toxic-ities are not less harmful than the risks associated with

surgery In the previous clinical trial RTOG 91–11 [3],

non-cancer-related death was more common among patients

treated with CRT than with RT alone in a further

follow-up, despite the higher rates of laryngeal preservation [4]

This suggests that patients cured by CRT need appropriate

management against late toxicity

Aspiration pneumonia is recognized as pneumonia

secondary to the inhalation of food particles, saliva, or

gastric acid Patients with HNC who have undergone

definitive CRT tend to have swallowing dysfunction due

to mucositis during the treatment period or due to

radiation-induced fibrosis of the oropharyngeal

muscula-ture after completion of the treatment [5] Szczesniak et

al [6] reported that approximately 52% of patients who

received RT and 69% who received CRT suffered from

dysphasia after treatment, and aspiration pneumonia

accounted for 19% of non-cancer-related deaths

Add-itionally, Xu et al [7] suggested that aspiration

pneumo-nia was a poor prognostic factor for patients with HNC

who received CRT Therefore, clinicians should assess

the risk of aspiration pneumonia in order to identify

pa-tients for whom efforts to prevent it should be

implemented

The purpose of this study was to identify clinical risk

factors for aspiration pneumonia after definitive CRT or

BRT for patients with advanced HNC In particular, we

focused on the cause-specific incidence of aspiration

pneumonia, taking competing events of death and

resec-tion of the primary lesion into account

Methods

Study population

Three hundred and forty patients with HNC who

re-ceived definitive concurrent CRT or BRT at Shizuoka

Cancer Center between August 2006 and April 2015

were identified from medical records Of these, 35

pa-tients with a recurrent or metastatic lesion or resection

of the primary lesion before CRT were excluded

Pa-tients with other malignancies were included only if

HNC was considered to be the factor most strongly

de-termining their prognosis Finally, 305 patients were

in-cluded in this analysis This study was approved by the

Institutional Review Committee of Shizuoka Cancer

Center (Shizuoka, Japan) and met the standards set forth

in the Declaration of Helsinki

Study covariates

We retrospectively collected data on the occurrence of as-piration pneumonia, time to onset of asas-piration pneumonia, and overall survival (OS) from the end of treatment Back-ground covariate candidates for factors predictive of aspir-ation pneumonia included the following: tumor site, age, gender, Eastern Cooperative Oncology Group (ECOG) per-formance status, body mass index, TNM staging according

to the AJCC/UICC TNM classification, tumor histology, smoking status, habitual alcoholic consumption, distance between the patients’ home and the hospital, family mem-bers in the same household, use of proton pump inhibitors (PPIs) or H2 blockers, use of angiotensin-converting en-zyme (ACE) inhibitors or angiotensin II receptor blockers (ARBs), use of sleeping pills and main feeding at the end of the treatment, presence of gastrostomy during the treat-ment, oral hygiene, serum albumin (ALB) and hemoglobin (Hb) levels before treatment, coexistence of other malig-nancies before treatment, and Charlson comorbidity index

We defined habitual alcoholic consumption as the drinking

of alcohol four or more days a week, and poor oral hygiene

as the presence of moderate or more severe dental plaque assessed by a dentist and/or a dental hygienist Charlson co-morbidity index is a tool for predicting mortality by classi-fying or weighting comorbidities [8]

We also collected the following treatment-related covar-iate data: presence or absence of induction chemotherapy, chemotherapy regimen, irradiation technique [conven-tional three-dimensional conformal radiation therapy (3D-CRT) or intensity-modulated radiation therapy (IMRT)], irradiation field, treatment efficacy evaluated according to Response Evaluation Criteria in Solid Tumors ver 1.1 [complete response (CR) or non-CR], mucositis and dys-phagia during treatment evaluated by Common Termin-ology Criteria for Adverse Events ver 4.0, and decreases

of ALB, Hb, and body weight after treatment

Aspiration pneumonia

Because it is sometimes difficult to clearly distinguish as-piration pneumonia from other types of pneumonia, dif-ferent definitions of aspiration pneumonia were used in previous studies [9–11] Therefore, in this study, we de-fined aspiration pneumonia as a clinical condition that met all of the following criteria: (i) Patients had both subjective and objective symptoms suggesting pneumo-nia Subjective symptoms included wet cough, sputum, and fever Objective symptoms included the presence of coarse crackles in the chest, elevated inflammatory markers (e.g white blood cell count or C-reactive pro-tein), or image findings (e.g infiltration on a chest X-ray

or consolidation in chest computed tomography) (ii) The presence of aspiration was suspected clinically (choking or delayed swallowing) or by endoscopic or video-fluorographic examinations (iii) No evidence of

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micro-organisms that cause atypical pneumonia, such as

Legionella and Mycoplasma

Statistical analysis

The cause-specific cumulative incidence of aspiration

pneumonia was estimated with nonparametric cumulative

incidence functions, taking competing events of death and

resection of the primary lesion into account To

investi-gate potential risk factors for aspiration pneumonia,

uni-variate analysis was carried out for all couni-variates using

Fisher’s exact test, and covariates showing statistical

sig-nificance were further analyzed using a multivariate

logis-tic regression model To construct a predictive model, we

automatically selected covariates extracted from univariate

analysis, and compared the goodness-of-fit among many

models on the basis of the stepwise Akaike information

criterion (AIC) method [12] The minimum value from

the AIC procedure allows us to select appropriate

pre-dictive factors to construct an optimal prepre-dictive model

objectively The concordance index to evaluate the

dis-criminatory ability of the model was calculated using the

final regression model [13]

The OS time was calculated from the date of

treat-ment end to the date of death due to any cause or to the

last date of confirmed survival Survival rates were

esti-mated using the Kaplan–Meier method To estimate the

association of covariates with overall survival, univariate

analysis was carried out using the log-rank test All

sta-tistically significant covariates in univariate analysis were

analyzed in multivariate analysis using the Cox

regres-sion model

All statistical tests were two-sided, and P≤ 0.05 was

considered significant Statistical analyses were

per-formed using EZR software (Saitama Medical Center,

Jichi Medical University, Saitama, Japan) [14]

Results

Among the 305 patients, 65 (21.3%) developed aspiration

pneumonia after CRT or BRT Patients’ baseline and

treatment-related characteristics are summarized in

Table 1 The median age of the patients was 65 years

(range 19–83) and 95.1% of them had ECOG PS of 0 to

1 Cisplatin, carboplatin, and cetuximab were

concur-rently used in 77.1, 13.7, and 9.2% of patients,

respect-ively Seventy-six (24.9%) of the patients received

induction chemotherapy, and 87.5% of them were

treated with the combination of docetaxel, cisplatin, and

fluorouracil Additionally, 96.0% of all patients had

re-ceived systematic oral care [15] since initiation of the

treatment Thirty-six (11.8%) patients had coexisting

ma-lignancies included multiple primary HNC, esophageal

cancer, gastric cancer, prostate cancer, lung cancer, and

renal cancer All of these cancers were found at an early

stage by routine endoscopic or computed tomography

screening After definitive CRT or BRT, 30 (9.8%) pa-tients underwent resection of the primary lesion and 45 (14.7%) underwent neck dissection for a residual lesion

or recurrence

The median time from the end of treatment to aspir-ation pneumonia events was 161 days (range 3–1623) The median follow-up time was 892 days The two-year cumulative incidences of aspiration pneumonia and competing events of death and resection of the primary lesion were 21.0% [95% confidence interval (CI) 16.4– 26.0%], 12.9% (9.2–17.4%), and 6.2% (3.7–9.5%), respect-ively (Fig 1)

Univariate and multivariate analyses identified five inde-pendent risk factors for aspiration pneumonia, namely, habitual alcoholic consumption, poor oral hygiene, coex-istence of other malignancies, hypoalbuminemia before treatment, and the use of sleeping pills at the end of treat-ment (Table 2) A difference in the types of sleeping pills (benzodiazepines or others) used was not associated with the onset of aspiration pneumonia (odds ratio 0.95, 95%

CI, 0.37–2.39, P = 1.00) Of 193 patients with poor oral hy-giene before treatment, 135 had been followed up by den-tists three months after the treatment In total, 87 of 135 patients in whom oral hygiene had improved three months after the treatment had a significantly lower fre-quency of aspiration pneumonia than 48 patients who had poor oral hygiene (18.3% vs 54.1%, P = 0.00003)

Next, we attempted to construct a predictive risk model of aspiration pneumonia from the results of uni-variate analysis As a result of AIC stepwise selection, six predictive factors, consisting of the five risk factors ex-tracted from the multivariate analysis and treatment effi-cacy (non-CR), were selected Although treatment efficacy was not identified as a statistically significant risk factor, AIC stepwise selection revealed that it was a good predictive factor for the model This predictive model well divided patients into low- (0–2 factors, n = 180), moderate- (3–4 factors, n = 103), and high-risk groups (5–6 factors, n = 22) by the number of predictive factors, for which the estimated two-year cumulative in-cidences of aspiration pneumonia were 3.0% (95% CI, 1.1–6.5%), 41.6% (31.0–51.8%), and 77.3% (51.4–90.5%), respectively (Fig 2) The concordance index was 0.797 Finally, we investigated the correlation between OS and the occurrence of aspiration pneumonia Survival curves adjusted for the covariates from a Cox propor-tional hazard model indicated that the occurrence of as-piration pneumonia tended to be associated with the risk of death, but this was not statistically significant (hazard ratio, 1.39; 95% CI, 0.85–2.27; P = 0.18) (Fig 3)

Discussion

The important goals of treatment in patients with HNC are not only a cure but also the preservation of quality

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Table 1 Patients’ characteristics

Age

Gender

ECOG performance status

Body mass index

Primary site

T-classification

N-classification

Tumor histology

Smoking status

Habitual alcoholic consumption

Table 1 Patients’ characteristics (Continued)

Distance from the hospital

Family members in the same household

Use of ACEi or ARB

Use of PPI or H 2 blocker

Oral hygiene before treatment

Coexistence of other malignancies

Comorbidity index

Serum albumin before treatment

Hemoglobin before treatment

Use of sleeping pills at the end of treatment

Main feeding at the end of treatment

Presence of gastrostomy during the treatment

Induction chemotherapy

Concurrent chemotherapy regimen

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of life post-treatment Although approximately 60–70%

of patients with HNC treated with CRT suffer from dys-phagia or aspiration as a late toxicity [16, 17], in previ-ous studies, the incidence of aspiration pneumonia within a year after CRT was found to differ, ranging from 5.4 to 23% [9, 17, 18] Furthermore, no differences

in the frequency of aspiration pneumonia were seen be-tween the different observation periods, despite the im-provement of radiation techniques and general management of CRT over the time This suggests that various factors other than aspiration are associated with the occurrence of aspiration pneumonia

To clarify the population at high risk of aspiration pneumonia after CRT or BRT, we investigated the tors predictive of aspiration pneumonia Several risk fac-tors for aspiration pneumonia in patients with HNC after CRT were reported in previous studies [7, 9, 17] However, evaluation of the long-term risk factors was often difficult in patients with HNC because these pa-tients’ characteristics varied according to the multimodal therapies that they had received, including surgery, CRT, and RT In particular, previous studies did not take sal-vage surgery after CRT into account Therefore, in these studies, there might not have been accurate estimates of the treatment-specific incidence of aspiration pneumo-nia after CRT To our knowledge, the current study is the first regarding specific risk factors and predictive models for aspiration pneumonia as a late toxicity in pa-tients with HNC undergoing definitive CRT or BRT

We intended to determine risk factors for aspiration pneumonia after CRT or BRT by estimating the cause-specific cumulative incidence To do this, we first per-formed cumulative incidence analysis, and regarded

Table 1 Patients’ characteristics (Continued)

Radiation technique

Irradiation field

Treatment efficacy

Body weight loss after treatment

Serum albumin decreasing post-treatment

Hemoglobin decreasing post-treatment

The worst mucositis grade during treatment

The worst dysphagia grade during treatment

Resection of primary lesion post-CRT or -BRT

Neck dissection post-CRT or -BRT

Abbreviations: ECOG Eastern Cooperative Oncology Group, SCC Squamous cell

carcinoma, ACEi Angiotensin-converting enzyme inhibitor, ARB Angiotensin II

receptor blocker, PPI Proton pump inhibitor, 3D-CRT Three-dimensional

conformal radiation therapy, IMRT Intensity-modulated radiation therapy, CR

Complete response, CRT Chemoradiotherapy, BRT Bio-radiotherapy

The normal range of laboratory data at our institution: Serum albumin (3.8–

5.2 g/dl), hemoglobin (male: 13.5 –17.6 g/dl, female: 11.3–15.2 g/dl)

Fig 1 Cumulative incidence of aspiration pneumonia and other competing risks including death and resection of primary lesion Vertical dashes indicate censored observations

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Table 2 Univariate and multivariate logistic regression analyses for risk factors of aspiration pneumonia

Age

Gender

ECOG performance status

Body mass index

Primary site

T-classification

N-classification

Tumor histology

Smoking status

Habitual alcoholic consumption

Distance from the hospital

Family members in the same household

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Table 2 Univariate and multivariate logistic regression analyses for risk factors of aspiration pneumonia (Continued)

Use of ACEi or ARB

Use of PPI or H 2 blocker

Oral hygiene before treatment

Coexistence of other malignancies

Comorbidity index

Serum albumin before treatment

Hemoglobin before treatment

Use of sleeping pills at the end of

treatment

Main feeding at the end of treatment

Presence of gastrostomy during the

treatment

Induction chemotherapy

Concurrent chemotherapy regimen

Radiation technique

Irradiation field

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Table 2 Univariate and multivariate logistic regression analyses for risk factors of aspiration pneumonia (Continued)

Treatment efficacy

Body weight loss after treatment

Serum albumin decreasing

post-treatment

Hemoglobin decreasing

post-treatment

The worst mucositis grade

during treatment

The worst dysphagia grade

during treatment

Abbreviations: ECOG Eastern Cooperative Oncology Group, SCC Squamous cell carcinoma, ACEi Angiotensin-converting enzyme inhibitor, ARB Angiotensin II receptor blocker, PPI Proton pump inhibitor, 3D-CRT Three-dimensional conformal radiation therapy, IMRT Intensity-modulated radiation therapy, CR Complete response The normal range of laboratory data at our institution: Serum albumin (3.8–5.2 g/dl), hemoglobin (male: 13.5–17.6 g/dl, female: 11.3–15.2 g/dl)

Fig 2 The estimated cumulative incidence of aspiration pneumonia according to the number of predictive factors Vertical dashes indicate censored observations

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resection of the primary lesion as a competing event.

Surgical procedures clearly affect swallowing function

For example, total laryngectomy reduces the risk of

as-piration and head and neck reconstruction changes

pa-tients’ ability to swallow [19, 20] Therefore, surgical

intervention after CRT/BRT may obscure the association

of aspiration with CRT or BRT On the other hand, the

effect of neck dissection on aspiration pneumonia has

been controversial For instance, Lango et al [21]

re-ported that radical neck dissection (RND) increased the

risk of feeding tube dependence in patients with HNC

who underwent RT or CRT On the other hand, Chapuy

et al [22] reported that types of neck dissection

includ-ing RND, modified RND, and selective neck dissection

(SND) did not aggravate swallowing function In this

study, 45 patients underwent neck dissection, 44 (97%)

of which underwent SND Our analysis suggested no

sig-nificant association between neck dissection and the

oc-currence of aspiration pneumonia (P = 0.23) Therefore,

we did not consider neck dissection as a competing

event in cumulative incidence analysis

Consistent with previous reports [23],

hypoalbumin-emia was again identified as a factor predictive of

aspir-ation pneumonia after CRT and BRT in our study The

novel predictive factors identified here were poor oral

hygiene, use of sleeping pills, coexistence of other

malig-nancies, and habitual alcohol consumption

Several studies have demonstrated that careful oral

management could reduce the risk of aspiration

pneu-monia in elderly people and patients with a history of

cerebral infarction [24, 25] However, few studies have

focused on the correlation between oral hygiene and the

risk of aspiration pneumonia in patients with HNC At our institution, patients with HNC undergoing RT have been routinely referred to dentists and received system-atic oral care during the treatment [15] Indeed, 96.0% of patients received oral evaluation before treatment in this cohort However, 35.6% of patients initially evaluated as having poor oral hygiene were still assessed as having this same status after the treatment This suggested that continuous oral management is required in high-risk pa-tients, even after treatment

Previous studies suggested that sleeping pills increased the risk of aspiration pneumonia [26, 27] Among these, benzodiazepines were especially associated with the in-duction of aspiration through gamma-amino-butyric acid type A (GABA-A) signaling in the lesser esophageal sphincter, in addition to inhibition of the central nervous system [28] However, in our study, benzodiazepines did not specifically increase the risk of aspiration pneumonia more than other sleeping pills Notably, 83 out of 94 (88.3%) patients who used sleeping pills at the end of the treatment continued to use them even after the treat-ment Al-Mamgani et al [29] demonstrated that 30.7%

of patients with nasopharyngeal cancer who received RT

or CRT had the complaint of insomnia during the treat-ment; however, approximately half of them recovered after the treatment These findings suggest that the un-necessary administration of sleeping pills might increase the risk of aspiration pneumonia for our patients Our data demonstrated that the coexistence of other malignancies was a risk factor for aspiration pneumonia

Of 11 patients who had multiple primary HNC or cer-vical esophageal cancers simultaneously treated by CRT with main HNC, 7 (63.6%) developed aspiration pneu-monia A previous report suggested that enlargement of the irradiation field increased the risk of aspiration pneumonia [30] Furthermore, 18 patients underwent surgical or endoscopic resection for esophageal and gas-tric cancer Of these, six (33.3%) developed aspiration pneumonia, three of whom developed it within one week resection Therefore, we speculated that post-surgical immunosuppression and anesthesia or sedation before endoscopy might deteriorate swallowing function Previous reports indicated that alcohol suppressed the cough reflex, reduced consciousness, and promoted gastro-esophageal reflux [31–33] Therefore, such com-plex factors induced by habitual alcohol consumption may be involved in the occurrence of aspiration pneumonia

Scheld et al [34] and Xu et al [7] reported that aspir-ation pneumonia was a significant prognostic factor Furthermore, Szczesniak et al [6] reported that aspir-ation pneumonia accounted for 19% of non-cancer-related deaths of patients with HNC who received CRT Therefore, we expected that aspiration pneumonia

Fig 3 Adjusted Kaplan –Meier curve illustrating overall survival from

the date of the end of the treatment among patients with head and

neck cancer who received chemoradiation or bio-radiation therapy

stratified according to whether or not they developed aspiration

pneumonia Vertical dashes indicate censored observations CI:

confidence interval, HR: hazard ratio

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would be strongly associated with patient survival

How-ever, our study did not show a statistically significant

dif-ference in survival between patients who developed

aspiration pneumonia and those who did not, probably

because of the relatively small number of deaths within

the short follow-up period

Our study had several limitations First, it involved a

retrospective analysis at a single institution Second,

dif-ferential diagnosis between aspiration pneumonia and

other types of pneumonia was often difficult because the

definitions of aspiration pneumonia varied among

previ-ous reports [9–11] Third, the median follow-up of

2.4 years was shorter than in previous studies [4, 7] The

ability of our predictive model might change upon a

long-term follow-up For example, because submucosal

remodeling and neurological disturbance slowly progress

after irradiation [35], irradiation might have a stronger

impact on the occurrence of aspiration pneumonia at a

later phase

Further studies are warranted to validate our predictive

model because of the retrospective nature of this study

However, the strength of our study is that almost all

pa-tients received standard chemotherapeutic regimens

con-taining platinum or cetuximab, with systematic supportive

care such as oral care Therefore, our predictive model

may be more useful for identifying patients at high risk for

aspiration pneumonia in recent clinical practice than

pre-vious evidences For example, we propose that clinicians

consider swallowing exercises for high- or moderate-risk

groups to improve their swallowing function and

subse-quently prevent aspiration pneumonia [35]

Conclusions

We investigated the cause-specific incidence and

identi-fied risk factors for aspiration pneumonia following

de-finitive CRT or BRT for patients with locally advanced

HNC The prediction of aspiration pneumonia may be

necessary to preserve the quality of life and extend life

expectancy for patients Long-term follow-up and

fur-ther prospective studies are needed to validate the

use-fulness of our predictive model

Abbreviations

3D-CRT: Three-dimensional conformal radiation therapy; ACE:

Angiotensin-converting enzyme; AIC: Akaike information criterion; ALB: Serum albumin;

ARBs: Angiotensin II receptor blockers; BRT: Bio-radiotherapy; CR: Complete

response; CRT: Chemoradiotherapy; ECOG: Eastern Cooperative Oncology

Group; GABA-A: Gamma-amino-butyric acid type A; Hb: Hemoglobin;

HNC: Head and neck cancer; IMRT: Intensity-modulated radiation therapy;

OS: Overall survival; PPIs: Proton pump inhibitors; RND: Radical neck

dissection; RT: Radiotherapy; SND: Selective neck dissection

Acknowledgements

Not applicable.

Funding

None.

Availability of data and material The data analyzed during the current study are available from the corresponding author on reasonable request.

Authors ’ contributions Conceptualization: SK, Writing an original draft: SK, Project administration: TY, Review and editing: TY, YO, AF, Formal analysis: KM, Supervision: HY, Investigation of data: SK, TY, SH, HO, TO, TO, TY, AT, TT, YY, YK, and All authors read and approved the final manuscript.

Competing interests The authors declare that they have no competing interests.

Consent for publication Not applicable.

Ethics approval and consent to participate This study was approved by the Institutional Review Committee of Shizuoka Cancer Center (Decision number 27-J104-27-1) and met the standards set forth in the Declaration of Helsinki Authors obtained written informed con-sent from the participants If it was difficult to get, authors provided the in-formation of this study and patients ’ right on the website or in a notice board at the hospital.

Author details

1 Division of Gastrointestinal Oncology, Shizuoka Cancer Center, 1007 Shimonagakubo, Nagaizumi, Sunto-gun, Shizuoka 411-8777, Japan.2Division

of Medical Oncology, Shizuoka Cancer Center, Sunto-gun, Shizuoka, Japan.

3

Division of Radiation Oncology and Proton Therapy, Shizuoka Cancer Center, Sunto-gun, Shizuoka, Japan 4 Division of Head and Neck Surgery, Shizuoka Cancer Center, Sunto-gun, Shizuoka, Japan.5Division of Dental and Oral Surgery, Shizuoka Cancer Center, Sunto-gun, Shizuoka, Japan 6 Clinical Research Center, Shizuoka Cancer Center, Sunto-gun, Shizuoka, Japan Received: 26 August 2016 Accepted: 10 January 2017

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